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Ostrovsky & Shunatova 2002 Paper in: Patrick N. Wyse Jackson & Mary E. Spencer Jones (eds) (2002) Annals of Bryozoology: aspects of the history of research on bryozoans. International Bryozoology Association, Dublin, pp. viii+381. COLONIAL BEHAVIOUR IN BRYOZOA 185 Colonial behaviour and group zooidal reactions in Bryozoa: history of research Andrew N. Ostrovsky* and Natalia N. Shunatova Department of Invertebrate Zoology, Faculty of Biology and Soil Science, St. Petersburg State University, Universitetskaja nab. 7/9, St. Petersburg, 199034, Russia *Present address: Institut für Geowissenschaften, Christian-Albrechts-Universität zu Kiel, Olshausenstr. 40, 24118 Kiel, Germany 1. Introduction 2. Early studies 3. Twentieth century studies 4. Conclusions 5. Acknowledgements 1. Introduction Investigations of modular systems encompass many colonial organisms with a high level of morphological and physiological integration. Bryozoan colonies are a very promising model in this respect, and studies of colonial behaviour are one of the approaches in evaluating the degree of colonial integration. Bryozoans demonstrate a variety of group behavioural reactions which are connected with different vital functions. Co-ordinated activities of polypides are regulated neurophysiologically, physiologically, structurally and, possibly, hormonally. Different manifestations of the regulatory mechanisms have been studied previously, and we here present a review that discusses the history of these investigations. 2. Early studies Henry Baker was probably the first who noted in passing colonial behavioural reactions in fresh-water bryozoans (possibly, Plumatella).1 Barthelemy Dumortier described retraction of all polypides in a colony of the phylactolaemate Lophopus crystallinus (Pallas) after a stimulus was applied to a ‘coenoecium’.2 Contact with a single lophophore resulted only in its retraction. The first description of synchronized polypide protrusion and retraction in colonies of marine bryozoans was published by George Johnston in 1838. In P.N. Wyse Jackson & M.E. Spencer Jones (eds), Annals of Bryozoology: aspects of the history of research on bryozoans (International Bryozoology Association, Dublin, 2002), pp. 185–199. 186 ANNALS OF BRYOZOOLOGY Similarly to Dumortier, he also mentioned that ‘if, when many [polypides] are expanded [in a colony], one is…touched with a sharp instrument, it alone feels an injury and retires, without any others being conscious of the danger’.3 But in spite of the intensive studies on different taxa of these colonial animals using live specimens (Hassall,4 Dalyell,5 Gosse,6 Busk,7 Allman,8 Smitt,9 ,10 Hyatt,11 Nitsche,12 -15 Vigelius,16 Kraepelin,17 Pergens,18 Oka,19 Proucho,20 Calvet,21 Gerwerzhagen,22 Borg,23 etc.)24 there are only occasional remarks concerning group autozooidal behaviour in the literature published. For instance, Thomas Hincks25 and Fritz Müller26 mentioned ‘common and simultaneous movements’ of the autozooids in the ctenostome Mimosella gracilis Hincks.27, 28 ,29 3. Twentieth century studies Folke Borg described removal of released eggs by their consecutive transference from lophophore to lophophore in a colony of the cheilostome Electra pilosa (Linnaeus).30 Ernst Marcus made some observations on bryozoan behaviour during his experiments on several species of both marine and fresh-water bryozoans, including the cheilostome E. pilosa, the ctenostome Farrella repens (Farre), and the phylactolaemates Cristatella mucedo Cuvier and Fredericella sultana (Blumenbach).31, 32 One of his main conclusions was that there is no colonial co-ordination in gymnolaemate Bryozoa, and that, as in the case of Johnston,33 no autozooid responded to a stimulus applied to any other.34 In contrast, the transmissions of stimuli from one member of a colony to another was demonstrated by Marcus for the phylactolaemates mentioned.35 Results of Marcus’s studies were regarded as being of the greatest importance by several authors36, 37, 38 in spite of the opinion of Georges Bronstein who claimed to have observed colonial responses in the ctenostome Bowerbankia sp.39 Also the data of Stanislaw Hiller, who described the interzooidal nervous connections in E. pilosa and E. crustulenta (Pallas) (both as Membranipora) and group polypide retractions after the stimulation of the frontal cystid wall,40 were considered as insufficient to cast doubt upon the conclusions of Marcus.41 Collective movements of entire zooids and whole zoarial branches resulting in a change of their orientation were investigated in detail by Lars Silén42 in ctenostomes of the genera Mimosella and Farrella and the cheilostome Kinetoskias correspondingly.43 However, Silén supported Marcus’s44 view, stating that mechanical stimulation of a zooid does not trigger any response from adjacent zooids.45, 46 Thus, the opinion about the absence of colonial co-ordination of zooidal activity survived for about 50 years in spite of the facts that there are momentary simultaneous polypide retractions after stimulation47-52 as well as movements of cheilostome bryozoan vibracula that can beat in unison.53-59 For instance, Silén believed that synchronous action of the vibracula in the cheilostome Caberea is a kind of metachronal chain reaction during which very long vibracular setae inevitably touch neighbouring ones that thereupon respond.60, 61, 62 Further investigations led researchers to suppose that the behaviour of Bryozoa is a very flexible and sensitive system of reactions that combines diverse individual and group COLONIAL BEHAVIOUR IN BRYOZOA 187 zooidal activities depending on the situation. At the present time, there are a lot of both morphological and behavioural evidences in favour of existence of the presumed colonial co-ordination in all main Recent bryozoan taxa. In addition to the anatomical data of earlier authors 63-71 many new facts that are indicative of nervous connections and transmission of nervous signals between zooids were obtained by Geneviève Lutaud,72- 80 who supported the hypothesis of interzooidal information spreading through a colony and leading to colonial responses.81 In the phylactolaemate Plumatella fungosa (Pallas) George Mackie recorded the phenomenon in which ‘the lophophores over wide regions become orientated by muscular action so that they point in the same direction’.82 He also mentioned co-ordinated withdrawal responses in Cristatella mucedo. Colonial behaviour and nervous responses were studied in some species of free-living cheilostome.83-87 Colonies under investigation showed a high degree of co-ordination of avicularian setae movement owing to which they were able to stop themselves being buried in sand, to return back to a normal position after being placed upside down, to travel across the aquarium preferably towards the light and to climb one over another.88 A high level of co-ordination was also recorded between autozooids, and between autozooids and avicularia, when feeding periods ending in simultaneous polypide retraction are alternated with simultaneous setal cleaning movement after which the colonial feeding is resumed. Co-ordinated avicularian activity in Recent lunulitiform bryozoans (Cupuladriidae) was also noted by Ernst and Eveline Marcus,89 Patricia Cook90 and Ronald Greeley.91 Judith Winston and Patricia Cook recorded synchronous movements of avicularian setae in different species of Cheilostomatida.92- 95 Collective activity of another type of bryozoan polymorphs was described by Lars Silén and Jean-Georges Harmelin who observed rocking and circular movements of the single tentacle of nanozooids in cyclostomes of the genera Plagioecia and Diplosolen.96 These movements were not synchronized but were simultaneous, and cleaned a colony surface after induced obstruction by silt. It was noted that the tentacles of nanozooids were the first to appear in the colony after strong disturbance, whereas autozooids expanded their lophophores much later. Similar ‘sentry’ behaviour performed solely by autozooids was also recorded in several cheilostomates.97 Some neurophysiological aspects of intra- and intercolonial co-ordination of behavioural responces were investigated in Membranipora membranacea (Linnaeus), Electra pilosa, Selenaria maculata (Busk) and Flustrellidra hispida (Fabricius).98-101 The long-term controversy (see above) was rejected at last. It was found in experiments that ‘mechanical [as well as electrical] stimulation of an extended lophophore…resulted solely in the retraction of that polypide’.102 In contrast, stimulation of the frontal membrane triggers ‘the immediate rapid withdrawal of all the extended lophophores within some distance of the zooid stimulated’.103, 104, 105 This is in good agreement with observations of Winston 188 ANNALS OF BRYOZOOLOGY who described group retractions during removal of large particles from a colony.106 Conduction of nerve pulses through the colony accompanied by quick consecutive retractions of polypides was proved both within the same colony107 -110 and within complexes of adjoining colonies.111 Moreover, such conduction was also shown in a representative of carnosan ctenostomes (F. hispida),112 although interzooidal nervous connections were not discovered by Lutaud who investigated Alcyonidium polyoum (Hassall).113 Michael Berry and Peter Hayward suggested that ‘the nervous activity responsible for co-ordinating locomotion would spread throughout the entire colony’ after their experiments with free-living S. maculata where strong illumination caused the colonies to start moving.114 Noticeably,
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